Abstract
High salinity is a major abiotic stressor that affects crop productivity and quality. While proper seedling growth is critical for crop reproduction under high salinity stress. Nowadays, genes/miRNAs expression is used for studying salinity stress response in rice seedlings. However, analysis of miRNA combined with gene expression is rare. To this end, we used miRNA-seq and gene expression profile to ascertain 6335 genes (3276 genes up-regulated, 3059 genes down-regulated) and 126 miRNAs (47 miRNAs up-regulated, 79 miRNAs down-regulated) that respond to salinity stress in rice seedlings. We then used these 126 miRNAs (including the novel miRNA osa-Chr12_1506) to identify 121 differentially expressed predicted target genes. In addition, we identified 34 miRNA-target RNA pairs, consisting of 9 differentially expressed miRNAs with complementary expression patterns. Combined with previous studies, we proposed a simple model for the molecular mechanism of a 12-h salinity stress response in rice seedlings. The findings lead to a deeper understanding of the function of miRNAs and genes that respond to salinity, and contributed to the elucidation of the complex mechanisms activated by salinity stress.
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References
Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121(2):207–221. https://doi.org/10.1016/j.cell.2005.04.004
Anders S (2010) Analysing RNA-seq data with the DESeq package. Mol Biol 43(4):1–17. https://doi.org/10.1186/gb-2010-11-10-r106
Barrera-Figueroa BE, Gao L, Wu Z, Zhou X, Zhu J, Jin H, Liu R, Zhu J-K (2012) High throughput sequencing reveals novel and abiotic stress-regulated microRNAs in the inflorescences of rice. BMC Plant Biol 12(1):132. https://doi.org/10.1186/1471-2229-12-132
Belamkar V, Weeks NT, Bharti AK, Farmer AD, Graham MA, Cannon SB (2014) Comprehensive characterization and RNA-seq profiling of the HD-zip transcription factor family in soybean (Glycine max) during dehydration and salt stress. BMC genomics 15(1):950. https://doi.org/10.1186/1471-2164-15-950
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc: Ser B (Methodol). https://doi.org/10.2307/2346101
Bottino MC, Rosario S, Grativol C, Thiebaut F, Rojas CA, Farrineli L, Hemerly AS, Ferreira PCG (2013) High-throughput sequencing of small RNA transcriptome reveals salt stress regulated microRNAs in sugarcane. PLoS One 8(3):e59423. https://doi.org/10.1371/journal.pone.0059423
Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301(5631):336–338. https://doi.org/10.1126/science.1085242
Choi JY, Seo YS, Kim SJ, Kim WT, Shin JS (2011) Constitutive expression of CaXTH3, a hot pepper xyloglucan endotransglucosylase/hydrolase, enhanced tolerance to salt and drought stresses without phenotypic defects in tomato plants (Solanum lycopersicum cv. Dotaerang). Plant Cell Rep 30(5):867–877. https://doi.org/10.1007/s00299-010-0989-3
Chuck G, Cigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39(4):544–549. https://doi.org/10.1038/ng2001
Claus H (2003) Laccases and their occurrence in prokaryotes. Arch Microbiol 179(3):145–150. https://doi.org/10.1007/s00203-002-0510-7
Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Curr Opin Plant Biol 3(2):117–124
Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103(1):29–38. https://doi.org/10.1093/aob/mcn205
Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135(1):1–9. https://doi.org/10.1016/S0168-9452(98)00025-9
Flowers T (2004) Improving crop salt tolerance. J Exp Bot 55(396):307–319. https://doi.org/10.1093/jxb/erh003
Frazier TP, Sun G, Burklew CE, Zhang B (2011) Salt and drought stresses induce the aberrant expression of microRNA genes in tobacco. Mol Biotechnol 49(2):159–165. https://doi.org/10.1007/s12033-011-9387-5
Gao P, Bai X, Yang L, Lv D, Pan X, Li Y, Cai H, Ji W, Chen Q, Zhu Y (2011) osa-MIR393: a salinity-and alkaline stress-related microRNA gene. Mol Biol Rep 38(1):237–242. https://doi.org/10.1007/s11033-010-0100-8
Ghosh N, Adak M, Ghosh P, Gupta S, Gupta DS, Mandal C (2011) Differential responses of two rice varieties to salt stress. Plant Biotechnol Rep 5(1):89–103. https://doi.org/10.1007/s11816-010-0163-y
Grassmann J, Hippeli S, Elstner EF (2002) Plant’s defence and its benefits for animals and medicine: role of phenolics and terpenoids in avoiding oxygen stress. Plant Physiol Biochem 40(6):471–478. https://doi.org/10.1016/S0981-9428(02)01395-5
Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Takabe T, Takabe T (2000) Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Mol Biol 43(1):103–111. https://doi.org/10.1023/A:1006408712416 PMID: 10949377
Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276(11):3148–3162. https://doi.org/10.1111/j.1742-4658.2009.07033.x
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53. https://doi.org/10.1146/annurev.arplant.57.032905.105218
Kantar M, Lucas SJ, Budak H (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233(3):471–484. https://doi.org/10.1007/s00425-010-1309-4
Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13(4):889–905. https://doi.org/10.1105/tpc.13.4.889
Kumar K, Kumar M, Kim S-R, Ryu H, Cho Y-G (2013) Insights into genomics of salt stress response in rice. Rice 6(1):27. https://doi.org/10.1186/1939-8433-6-27
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10(3):R25. https://doi.org/10.1186/gb-2009-10-3-r25
Li H, Dong Y, Yin H, Wang N, Yang J, Liu X, Wang Y, Wu J, Li X (2011) Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biol 11(1):170. https://doi.org/10.1186/1471-2229-11-170
Li B, Duan H, Li J, Deng XW, Yin W, Xia X (2013) Global identification of miRNAs and targets in Populus euphratica under salt stress. Plant Mol Biol 81(6):525–539. https://doi.org/10.1007/s11103-013-0010-y
Liang M, Haroldsen V, Cai X, Wu Y (2006) Expression of a putative laccase gene, ZmLAC1, in maize primary roots under stress. Plant Cell Environ 29(5):746–753. https://doi.org/10.1111/j.1365-3040.2005.01435.x
Liu G, Greenshields DL, Sammynaiken R, Hirji RN, Selvaraj G, Wei Y (2007) Targeted alterations in iron homeostasis underlie plant defense responses. J Cell Sci 120(4):596–605. https://doi.org/10.1242/jcs.001362
Lu W, Li J, Liu F, Gu J, Guo C, Xu L, Zhang H, Xiao K (2011) Expression pattern of wheat miRNAs under salinity stress and prediction of salt-inducible miRNAs targets. Front Agric China 5(4):413–422. https://doi.org/10.1007/s11703-011-1133-z
Mal C, Deb A, Aftabuddin M, Kundu S (2013) miRNA mediated regulation of rice (Oryza sativa) genome. IFAC Proc Vol 46(31):95–100. https://doi.org/10.3182/20131216-3-IN-2044.00059
Martin C, Smith AM (1995) Starch biosynthesis. Plant Cell 7(7):971. https://doi.org/10.1105/tpc.7.7.971
Molina C, Zaman-Allah M, Khan F, Fatnassi N, Horres R, Rotter B, Steinhauer D, Amenc L, Drevon J-J, Winter P (2011) The salt-responsive transcriptome of chickpea roots and nodules via deepSuperSAGE. BMC Plant Biol 11(1):31. https://doi.org/10.1186/1471-2229-11-31
Park S-H, Chung PJ, Juntawong P, Bailey-Serres J, Kim YS, Jung H, Bang SW, Kim Y-K, Do Choi Y, Kim J-K (2012) Posttranscriptional control of photosynthetic mRNA decay under stress conditions requires 3′ and 5′ untranslated regions and correlates with differential polysome association in rice. Plant Physiol 159(3):1111–1124. https://doi.org/10.1104/pp.112.194928
Radomiljac JD, Whelan J, van der Merwe M (2013) Coordinating metabolite changes with our perception of plant abiotic stress responses: emerging views revealed by integrative—omic analyses. Metabolites 3(3):761–786. https://doi.org/10.3390/metabo3030761
Rama S, Annapurna B, Mukesh J (2016) Transcriptome analysis in different rice cultivars provides novel insights into desiccation and salinity stress responses: [J]. Sci Rep 6:23719. https://doi.org/10.1038/srep23719
Ray DK, Ramankutty N, Mueller ND, West PC, Foley JA (2012) Recent patterns of crop yield growth and stagnation. Nat Commun 3:1293. https://doi.org/10.1038/ncomms2296
Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110(4):513–520. https://doi.org/10.1016/S0092-8674(02)00863-2
Schmidt R, Mieulet D, Hubberten H-M, Obata T, Hoefgen R, Fernie AR, Fisahn J, San Segundo B, Guiderdoni E, Schippers JH (2013) SALT-RESPONSIVE ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. Plant Cell 25(6):2115–2131. https://doi.org/10.1105/tpc.113.113068
Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8(4):517–527. https://doi.org/10.1016/j.devcel.2005.01.018
Shankar R, Bhattacharjee A, Jain M (2016) Transcriptome analysis in different rice cultivars provides novel insights into desiccation and salinity stress responses [J]. Sci Rep 6:23719. https://doi.org/10.1038/srep23719
Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16(8):2001–2019. https://doi.org/10.1105/tpc.104.022830
Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7(11):847–859. https://doi.org/10.1038/nrm2020
Travers AA, Burgess RR (1969) Cyclic re-use of the RNA polymerase sigma factor. Nature 222(5193):537–540. https://doi.org/10.1038/222537a0
Wang H, Miyazaki S, Kawai K, Deyholos M, Galbraith DW, Bohnert HJ (2003) Temporal progression of gene expression responses to salt shock in maize roots. Plant Mol Biol 52(4):873–891. https://doi.org/10.1023/A:1025029026375
Wanichananan P, Kirdmanee C, Vutiyano C (2003) Effect of salinity on biochemical and physiological characteristics in correlation to selection of salt-tolerance in aromatic rice (Oryza sativa L.). Scienceasia 29(4):333–339. https://doi.org/10.2306/scienceasia1513-1874.2003.29.333
Yan J, Gu Y, Jia X, Kang W, Pan S, Tang X, Chen X, Tang G (2012) Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24(2):415–427. https://doi.org/10.1105/tpc.111.094144
Yeo A, Yeo M, Flowers S, Flowers T (1990) Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance. TAG. Theor Appl Genet 79(3):377–384. https://doi.org/10.1007/BF01186082
Zhao Y, Ji S, Wang J, Huang J, Zheng P (2014) mRNA-Seq and microRNA-seq whole-transcriptome analyses of rhesus monkey embryonic stem cell neural differentiation revealed the potential regulators of rosette neural stem cells. DNA Res 21(5):541–554. https://doi.org/10.1093/dnares/dsu019
Zhou M, Gu L, Li P, Song X, Wei L, Chen Z, Cao X (2010) Degradome sequencing reveals endogenous small RNA targets in rice (Oryza sativa L. ssp. indica). Front Biol 5(1):67–90. https://doi.org/10.1007/s11515-010-0007-8
Zhou Y, Yang P, Cui F, Zhang F, Luo X, Xie J (2016) Transcriptome analysis of salt stress responsiveness in the seedlings of dongxiang wild rice (Oryza rufipogon griff.). PLoS One 11(1):e0146242. https://doi.org/10.1371/journal.pone.0146242
Acknowledgements
This research was supported by the National Science Fund of China (nos. 31070276 and 31270360). We would like to thank Guang Zhou Gene Denonvo Bio-tech for supporting the analysis of partial data.
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Raw reads of the transcriptome have been deposited into the NCBI Short Read Archive (SRA, http://www.ncbi.nlm.nih.gov/sra/) under the accession numbers: SRR2886945, SRR2786811, SRR2890846 and SRR2890862.
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Communicated by Y. Wang.
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11738_2017_2570_MOESM4_ESM.xlsx
Supplementary material 4 (XLSX 11 kb) Table S1: The statistics of Solexa Sequencing and the mapping results of miRNA-seq reads
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Supplementary material 5 (XLSX 10 kb) Table S2: Specific primers information for qRT-PCR and miRNAs for stem-loop RT-PCR
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Supplementary material 7 (XLSX 24 kb) Table S4: miRNAs and their target genes respond to salinity stress in rice seedlings
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Wang, Q., Geng, T., Zhu, S. et al. Analysis of miRNA-seq combined with gene expression profile reveals the complexity of salinity stress response in Oryza sativa . Acta Physiol Plant 39, 272 (2017). https://doi.org/10.1007/s11738-017-2570-y
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DOI: https://doi.org/10.1007/s11738-017-2570-y